Equipped for success: genomes and metabolomes of the European Amanita muscaria are conserved in its novel South African range

Authors: NICKLES, GRANT - University Of Wisconsin; STOKES, CECELIA - University Of Wisconsin; NARH, DEBORAH - Stanford University; LYNN, KIRA - University Of Pretoria; FUQUA, SAVANNAH - University Of Arizona; BRYAN, CORBIN - University Of Wisconsin; ALLEN, BROOKE - University Of Mississippi; BIVINS, CHRISTOPHER - University Of California; BOK, JIN-WOO - University Of Wisconsin; BREWER, STEPHEN - University Of Mississippi; BUTHELEZI, SIKELELA - University Of Pretoria; CLARK, JAHIYA - University Of California Santa Cruz; COON, KERRI - University Of Wisconsin; CORBY, LAUREN - Jackson State University; COETZEE, MARTIN - University Of Pretoria; DEWING, CLAUDETTE - University Of Pretoria; DUONG, TUAN - University Of Pretoria; HARRIS, MATTHEW - University Of Pretoria; KELLER, NANCY - University Of Wisconsin; KOPOTSA, KATLEGO - University Of Pretoria; LANE, FRANCES - University Of Pretoria; NICHOLS, HOLLY - University Of Wisconsin; NIEUWOUDT, ALANDIE - University Of Pretoria; NUNEZ, MARTIN - University Of Houston; MEDINA MUNOZ, MIGUEL - University Of Wisconsin; PARK, SUNG-CHUL - University Of Wisconsin; PHAM, NAM - University Of Pretoria; RYAN, KAETLYN - University Of Wisconsin; SOLIS, MYRIAM - University Of Pretoria; VILGALYS, RYTAS - Duke University; WALLACE, JASMINE - Mississippi Valley State University; WANG, YEN-WEN - Yale University; WINGFIELD, BRENDA - University Of Pretoria; WINGFIELD, MICHAEL - University Of Pretoria; ZALLEK, TAYLOR - University Of Minnesota; ZAMANIAN, MOSTAGA - University Of Wisconsin; HOEKSEMA, JASON - University Of Mississippi; Drott, Milton; PRINGLE, ANNE - University Of Wisconsin; WORLEY, TRAVIS - University Of Wisconsin

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/19/2026
Publication Date: 2/17/2026
Citation: Nickles, G.R., Stokes, C.K., Narh, D.L., Lynn, K.M., Fuqua, S.R., Bryan, C., Allen, B.M., Bivins, C.P., Bok, J., Brewer, S.J., Buthelezi, S.T., Clark, J., Coon, K., Corby, L., Coetzee, M., Dewing, C., Duong, T., Harris, M., Keller, N., Kopotsa, K., Lane, F., Nichols, H., Nieuwoudt, A., Nunez, M., Medina Munoz, M., Park, S., Pham, N.Q., Ryan, K.T., Solis, M., Vilgalys, R., Wallace, J., Wang, Y., Wingfield, B., Wingfield, M., Zallek, T., Zamanian, M., Hoeksema, J., Drott, M.T., Pringle, A., Worley, T. 2026. Equipped for success: genomes and metabolomes of the European Amanita muscaria are conserved in its novel South African range. New Phytologist. 250(3):1863-1883. https://doi.org/10.1111/nph.71064.
DOI: https://doi.org/10.1111/nph.71064

Interpretive Summary: The spread of fungi through human movement of plants is increasingly leading to the emergence of invasive fungi across the globe. The ways in which emerging fungi adapt to new environments is poorly understood leaving many questions about strategies to mitigate the spread of these organisms. Here we investigated one of the oldest known introductions: a European fungus that was transmitted to the pine plantations of South Africa. We use historical records to demonstrate that this transmission likely occurred over 150 years ago through the movement of infected hosts and their associated soils. Genome sequencing supports these historical inferences. Analysis of gene content demonstrates that production of toxic secondary metabolites has been strongly conserved in the invasive range suggesting that toxin genes from native ranges may be re-appropriated in the invasive range. Indeed, while toxin resistance is known to exist among antagonists in the native range, we confirm that naive fungal agonists are highly susceptible to these toxins. Overall these results demonstrates that the introduction of fungi to new places may be difficult to control as naive agonists will be less likely to control the spread of these fungi and their newly introduced 'weapons'.

Technical Abstract: Plants and soils have been moved around the world for centuries, but invasive mushrooms receive scant attention. The Amanita muscaria species complex was introduced to South Africa in the context of forestry, but its origins, ecology, and recent evolution are unstudied. We sequenced the genomes of 25 Northern and Southern Hemisphere Amanita muscaria s.l., built phylogenies, and reconstructed its South African history. We identified the biosynthetic gene clusters (BGCs) encoding specialized metabolites (SMs). We subsequently extracted mushrooms’ metabolites and used mass spectrometry data to group SMs into unique molecular families (MFs). We tested metabolites for bioactivity against diverse microbes and animals. We identify Europe as the origin of South African A. muscaria. A highly conserved suite of BGCs are found in nearly all European and African genomes, and only 13 of 273 MFs are unique to South Africa. Metabolites extracted from all mushrooms kill nematodes and flies. The nearly global distribution of A. muscaria results from multiple introductions of a single European clade to the Southern Hemisphere. Despite its long history in South Africa, the fungus has not lost any of its BGCs, suggesting a conservation of function(s) across multiple continents.